Gram-negative soil bacteria (rhizobia) within the Rhizobiaceae phylogenetic family (a-proteobacteria) have the unique ability to infect and establish a nitrogen-fixing symbiosis on the roots of leguminous plants. This symbiosis is of agronomic importance, reducing the need for nitrogen fertilizer for agriculturally important plants (e.g. soybean and alfalfa). The establishment of the symbiosis involves a complex interplay between host and symbiont, resulting in the formation of a novel organ, the nodule, which the bacteria colonize as intracellular symbionts. This review focuses on the most recent discoveries relating to how this symbiosis is established. Two general developments have contributed to the recent explosion of research progress in this area: first, the adoption of two genetic model legumes, Medicago truncatula and Lotus japonicus, and second, the application of modern methods in functional genomics (e.g. transcriptomic, proteomic and metabolomic analyses).
IntroductionNodulation is a highly host-specific interaction in which, with few exceptions, specific rhizobial strains infect a limited range of plant hosts. Plants secrete (iso)flavonoids that are recognized by the compatible bacteria, resulting in the induction of nodulation genes. These nodulation genes encode enzymes that synthesize a specific lipochitin nodulation signal (Nod signal), which activates many of the early events in the root hair infection process [1][2][3][4][5]. During the infection process, the bacteria enter the plant via the root epidermis and induce the reprogramming of root cortical cell development and the formation of a nodule. In the most well-studied cases, infection occurs through root hairs. The first observable event in the infection process is the curling of the root hair, which likely occurs through the gradual and constant reorientation of the direction of root hair growth. The bacteria become enclosed within the root hair curl where the plant cell wall is degraded, the cell membrane is invaginated and an intracellular tubular structure (i.e. the infection thread) is initiated. It is within this infection thread that the bacteria enter the root hair cell and eventually ramify into the root cortex. Before the infection thread reaches the base of the root hair cell, the root cortical cells are induced to de-differentiate, activating their cell cycle and causing them to divide to form the nodule primordium. In addition to the cortical cells, pericycle cells are also activated and undergo some cell divisions. When the infection thread reaches the cells of the developing primordium, the bacteria are released into cells via endocytosis. Inside a plant cell, the bacteria are enclosed in vacuole-like structures (symbiosomes) in which they differentiate into bacteroids. It is within these symbiosomes that the bacteria convert N 2 to NH 3 . The nodule is a true organ in which there is cellular specialization. For example, in addition to infected plant cells, uninfected plant cells also carry out the function of nitrogen as...